Genome evolution and the emergence of pathogenicity in avian Escherichia coli

• Published in: Nature communications Vol. 12; no. 1; pp. 765 - 13
• Main Authors: Mageiros, Leonardos, Méric, Guillaume, Bayliss, Sion C, Pensar, Johan, Pascoe, Ben, Mourkas, Evangelos, Calland, Jessica K, Yahara, Koji, Murray, Susan, Wilkinson, Thomas S, Williams, Lisa K, Hitchings, Matthew D, Porter, Jonathan, Kemmett, Kirsty, Feil, Edward J, Jolley, Keith A, Williams, Nicola J, Corander, Jukka, Sheppard, Samuel K
• Format: Journal Article
• Language: English; Norwegian
• Published: England Nature Publishing Group 03.02.2021; Nature Portfolio; Nature Publishing Group UK
• Subjects: Animal welfare; Animals; Antimicrobial resistance; Bacteria; Chickens; Colibacillosis; Disease; Disseminated infection; Divergence; E coli; Escherichia coli; Escherichia coli - classification; Escherichia coli - genetics; Escherichia coli - pathogenicity; Escherichia coli Infections - diagnosis; Escherichia coli Infections - microbiology; Escherichia coli Infections - prevention & control; Etiology; Evolution, Molecular; Food production; Gene transfer; Genes; Genes, Bacterial; Genetic Variation; Genome, Bacterial - genetics; Genome-Wide Association Study - methods; Genomics; Genotype; Heat shock; Horizontal transfer; Humans; Infections; Lipopolysaccharides; Metabolism; Pathogenicity; Pathogens; Phylogeny; Poultry; Poultry Diseases - diagnosis; Poultry Diseases - microbiology; Poultry Diseases - prevention & control; Shock resistance; Systemic diseases; Toxicity; Virulence; Virulence - genetics
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-021-20988-w

Chickens are the most common birds on Earth and colibacillosis is among the most common diseases affecting them. This major threat to animal welfare and safe sustainable food production is difficult to combat because the etiological agent, avian pathogenic Escherichia coli (APEC), emerges from ubiquitous commensal gut bacteria, with no single virulence gene present in all disease-causing isolates. Here, we address the underlying evolutionary mechanisms of extraintestinal spread and systemic infection in poultry. Combining population scale comparative genomics and pangenome-wide association studies, we compare E. coli from commensal carriage and systemic infections. We identify phylogroup-specific and species-wide genetic elements that are enriched in APEC, including pathogenicity-associated variation in 143 genes that have diverse functions, including genes involved in metabolism, lipopolysaccharide synthesis, heat shock response, antimicrobial resistance and toxicity. We find that horizontal gene transfer spreads pathogenicity elements, allowing divergent clones to cause infection. Finally, a Random Forest model prediction of disease status (carriage vs. disease) identifies pathogenic strains in the emergent ST-117 poultry-associated lineage with 73% accuracy, demonstrating the potential for early identification of emergent APEC in healthy flocks.